Examination of the nickel site structure and reaction mechanism in Streptomyces seoulensis superoxide dismutase

Suranjan B. Choudhury, Jin Won Lee, Gerard Davidson, Yang In Yim, Kurethara Bose, Manju L. Sharma, Sa Ouk Kang, Diane E. Cabelli, Michael J. Maroney

Research output: Contribution to journalArticle

122 Citations (Scopus)

Abstract

Superoxide dismutases are metalloenzymes involved in protecting cells from oxidative damage arising from superoxide radical or reactive oxygen species produced from superoxide. Examples of enzymes containing Cu, Mn, and Fe as the redox-active metal have been characterized. Recently, a SOD containing one Ni atom per subunit was reported. The amino acid sequence of the NiSOD deduced from the nucleotide sequence of the structural gene sodN from Streptomyces seoulensis is reported and has no homology with other SODs. X-ray absorption spectroscopic studies coupled with EPR of the Ni center show that the Ni in the oxidized (as isolated) enzyme is in a five-coordinate site composed of three S-donor ligands, one N-donor, and one other O- or N-donor. This unique coordination environment is modified by the loss of one N- (or O- ) donor ligand in the dithionite-reduced enzyme. The NiSOD activity was determined by pulse radiolysis, and a value of k(cat) = 1.3 x 109 M-1 s- 1 per Ni was obtained. The rate is pH sensitive and drops off rapidly above pH 8. The results characterize a novel class of metal center active in catalyzing the redox chemistry of superoxide and, when placed in context with other nickel enzymes, suggest that thiolate ligation is a prerequisite for redox-active nickel sites in metalloenzymes.

Original languageEnglish
Pages (from-to)3744-3752
Number of pages9
JournalBiochemistry
Volume38
Issue number12
DOIs
StatePublished - 1999 Mar 23

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Streptomyces
Nickel
Superoxide Dismutase
Superoxides
Oxidation-Reduction
Enzymes
Metals
Pulse Radiolysis
Ligands
Dithionite
Radiolysis
X ray absorption
Ligation
Paramagnetic resonance
Amino Acid Sequence
Reactive Oxygen Species
Catalytic Domain
Nucleotides
Genes
X-Rays

Cite this

Choudhury, S. B., Lee, J. W., Davidson, G., Yim, Y. I., Bose, K., Sharma, M. L., ... Maroney, M. J. (1999). Examination of the nickel site structure and reaction mechanism in Streptomyces seoulensis superoxide dismutase. Biochemistry, 38(12), 3744-3752. https://doi.org/10.1021/bi982537j
Choudhury, Suranjan B. ; Lee, Jin Won ; Davidson, Gerard ; Yim, Yang In ; Bose, Kurethara ; Sharma, Manju L. ; Kang, Sa Ouk ; Cabelli, Diane E. ; Maroney, Michael J. / Examination of the nickel site structure and reaction mechanism in Streptomyces seoulensis superoxide dismutase. In: Biochemistry. 1999 ; Vol. 38, No. 12. pp. 3744-3752.
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Choudhury, SB, Lee, JW, Davidson, G, Yim, YI, Bose, K, Sharma, ML, Kang, SO, Cabelli, DE & Maroney, MJ 1999, 'Examination of the nickel site structure and reaction mechanism in Streptomyces seoulensis superoxide dismutase', Biochemistry, vol. 38, no. 12, pp. 3744-3752. https://doi.org/10.1021/bi982537j

Examination of the nickel site structure and reaction mechanism in Streptomyces seoulensis superoxide dismutase. / Choudhury, Suranjan B.; Lee, Jin Won; Davidson, Gerard; Yim, Yang In; Bose, Kurethara; Sharma, Manju L.; Kang, Sa Ouk; Cabelli, Diane E.; Maroney, Michael J.

In: Biochemistry, Vol. 38, No. 12, 23.03.1999, p. 3744-3752.

Research output: Contribution to journalArticle

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T1 - Examination of the nickel site structure and reaction mechanism in Streptomyces seoulensis superoxide dismutase

AU - Choudhury, Suranjan B.

AU - Lee, Jin Won

AU - Davidson, Gerard

AU - Yim, Yang In

AU - Bose, Kurethara

AU - Sharma, Manju L.

AU - Kang, Sa Ouk

AU - Cabelli, Diane E.

AU - Maroney, Michael J.

PY - 1999/3/23

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N2 - Superoxide dismutases are metalloenzymes involved in protecting cells from oxidative damage arising from superoxide radical or reactive oxygen species produced from superoxide. Examples of enzymes containing Cu, Mn, and Fe as the redox-active metal have been characterized. Recently, a SOD containing one Ni atom per subunit was reported. The amino acid sequence of the NiSOD deduced from the nucleotide sequence of the structural gene sodN from Streptomyces seoulensis is reported and has no homology with other SODs. X-ray absorption spectroscopic studies coupled with EPR of the Ni center show that the Ni in the oxidized (as isolated) enzyme is in a five-coordinate site composed of three S-donor ligands, one N-donor, and one other O- or N-donor. This unique coordination environment is modified by the loss of one N- (or O- ) donor ligand in the dithionite-reduced enzyme. The NiSOD activity was determined by pulse radiolysis, and a value of k(cat) = 1.3 x 109 M-1 s- 1 per Ni was obtained. The rate is pH sensitive and drops off rapidly above pH 8. The results characterize a novel class of metal center active in catalyzing the redox chemistry of superoxide and, when placed in context with other nickel enzymes, suggest that thiolate ligation is a prerequisite for redox-active nickel sites in metalloenzymes.

AB - Superoxide dismutases are metalloenzymes involved in protecting cells from oxidative damage arising from superoxide radical or reactive oxygen species produced from superoxide. Examples of enzymes containing Cu, Mn, and Fe as the redox-active metal have been characterized. Recently, a SOD containing one Ni atom per subunit was reported. The amino acid sequence of the NiSOD deduced from the nucleotide sequence of the structural gene sodN from Streptomyces seoulensis is reported and has no homology with other SODs. X-ray absorption spectroscopic studies coupled with EPR of the Ni center show that the Ni in the oxidized (as isolated) enzyme is in a five-coordinate site composed of three S-donor ligands, one N-donor, and one other O- or N-donor. This unique coordination environment is modified by the loss of one N- (or O- ) donor ligand in the dithionite-reduced enzyme. The NiSOD activity was determined by pulse radiolysis, and a value of k(cat) = 1.3 x 109 M-1 s- 1 per Ni was obtained. The rate is pH sensitive and drops off rapidly above pH 8. The results characterize a novel class of metal center active in catalyzing the redox chemistry of superoxide and, when placed in context with other nickel enzymes, suggest that thiolate ligation is a prerequisite for redox-active nickel sites in metalloenzymes.

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